A bacterium from a mountain lake harvests light using both proton-pumping xanthorhodopsins and bacteriochlorophyll-based photosystems

Abstract

Photoheterotrophic bacteria harvest light energy using either proton-pumping rhodopsins or bacteriochlorophyll (BChl)-based photosystems. The bacterium Sphingomonas glacialis AAP5 isolated from the alpine lake Gossenköllesee contains genes for both systems. Here, we show that BChl is expressed between 4°C and 22°C in the dark, whereas xanthorhodopsin is expressed only at temperatures below 16°C and in the presence of light. Thus, cells grown at low temperatures under a natural light–dark cycle contain both BChl-based photosystems and xanthorhodopsins with a nostoxanthin antenna. Flash photolysis measurements proved that both systems are photochemically active. The captured light energy is used for ATP synthesis and stimulates growth. Thus, S. glacialis AAP5 represents a chlorophototrophic and a retinalophototrophic organism. Our analyses suggest that simple xanthorhodopsin may be preferred by the cells under higher light and low temperatures, whereas larger BChl-based photosystems may perform better at lower light intensities. This indicates that the use of two systems for light harvesting may represent an evolutionary adaptation to the specific environmental conditions found in alpine lakes and other analogous ecosystems, allowing bacteria to alternate their light-harvesting machinery in response to large seasonal changes of irradiance and temperature.

Declines in ice cover are accompanied by light limitation responses and community change in freshwater diatoms

“…The DE genes within COG category P also largely belong to the Mediophyceae class, comprising ~40% of the annotated genes ( Supplemental Figures 15 and 16 ). Two proton-pumping rhodopsin genes (PPRs; COG category S), which were most recently found to be a light-driven, retinal-based alternative to classical phototrophy in a cold-adapted freshwater photosynthetic bacterium [ 64 ], significantly increased in expression within planktonic ice-free diatom communities ( Figure 6A , Supplemental Figure 17A ). Further, the expression of 9 additional diatom PPRs increased within the ice-free water column, though they fell short of our statistical differential expression cutoff ( Supplemental Figure 17B ).…”

“…However, compared to studies in the marine literature [ 80 , 83 , 85–88 ], PPRs are understudied in fresh waters. Yet, it has recently been suggested that PPRs may play a role in fresh waters: a photoheterotrophic bacterium isolated from an alpine lake used PPRs as an alternative phototrophy mechanism [ 64 ]. The authors of that study hypothesized that the contribution of PPRs to energy generation was linked to ice cover.…”

Diurnal cycles drive rhythmic physiology and promote survival in facultative phototrophic bacteria

“…The conspicuous light-driven oscillations in optical density we detected in batch cultures of Porphyrobacter sp. ULC335 have never been reported or studied so far in AAnP-competent bacteria, with the exception of Sphingomonas glacialis AAP5, recently isolated from an alpine lake, which combines retinalophototrophy and chlorophotoptrophy [71]. In our case, the oscillations involve an increase in density during light phases and a decrease in density during dark phases.…”

Photochemistry of the Retinal Chromophore in Microbial Rhodopsins

“…72 Interestingly, XR from Sphingomonas glacialis AAP5 isolated from the alpine lake Gossenkollesee was also found to use a rare 2,3-hydroxycarotenoid, nostoxanthin, as an antenna pigment. 73 Although these findings suggest that XR is not the only rhodopsin using an antenna carotenoid, most microbial rhodopsins were thought not to bind antenna carotenoids. However, functional metagenomics revealed that several XRs and proteorhodopsins (PRs) bind 3-hydroxylcarotenoid, such as lutein and zeaxanthin (ZXN), indicating that these 3hydroxylcarotenoids, which are more prevalent than SXN, are used by XRs and PRs of diverse bacteria.…”

“…Following XR, Gloeobacter rhodopsin (GR) from a cyanobacterium, Gloeobacter violaceus , which belongs to the XR subfamily, was also found capable of binding a different type of 4-ketocarotenoid, echinenone, and to perform EET . Interestingly, XR from Sphingomonas glacialis AAP5 isolated from the alpine lake Gossenköllesee was also found to use a rare 2,3-hydroxycarotenoid, nostoxanthin, as an antenna pigment . Although these findings suggest that XR is not the only rhodopsin using an antenna carotenoid, most microbial rhodopsins were thought not to bind antenna carotenoids.…”